The smelly side of ant social life

Indian jumping ant female workers usually rely on smell to note the absence of a queen and step in. A gene mutation puts paid to all that

Harpegnathos worker ants interacting. Photo: Jürgen Liebig/ASU

Harpegnathos worker ants interacting. Photo: Jürgen Liebig/ASU

Ants rely on chemistry to ensure they know who’s who in the family Formicidae (that’s the one all ants belong to), and keeping out those who do not belong.

Those genetically engineered to lack a “sense of smell” became unable to communicate, forage or compete to be a queen, as their antennae and brain circuits failed to fully develop. Here, researchers successfully shut down a crucial portion of the Indian jumping ant’s olfactory system by using the CRISPR-Cas9 technology.

This finding, stemming from a recent study conducted by researchers at New York University, University of Pennsylvania, Vanderbilt University and Arizona State University, was published online in the journal Cell.

“While ant behavior does not directly extend to humans, we believe that this work promises to advance our understanding of social communication, with the potential to shape the design of future research into disorders like schizophrenia, depression or autism that interfere with it,” said corresponding author Claude Desplan, professor at New York University’s Department of Biology.

“We found that a species of ant may be the first model to enable in-depth functional analysis of genes that regulate social interaction in a complex society,” said study co-author Danny Reinberg, a professor with the NYU School of Medicine and investigator for the Howard Hughes Medical Institute.

Jürgen Liebig, an associate professor with ASU’s School of Life Sciences and expert in social insect societies, is also encouraged by the results.
“Having studied the behavioral plasticity, colony organization and chemical communication of the ant Harpegnathos saltator for more than two decades, I am happy to see that this charismatic species is finally maturing into a genetic model,” co-author Liebig said.

As has been shown before, the current results, too, are based on the fact that ants communicate through pheromones, secreted chemicals that trigger responses. Such odors are used to spread alarm as a predator approaches, leave a trail to food, indicate social (caste) status and signal readiness to mate, all within cooperative societies that achieve complex tasks. Ants can receive such signals because they have proteins called odorant receptors on their antennae, with each protein the right shape to bind to a specific odorant chemical.
 
For any odor or pheromone to be processed in an ant’s brain, however, past studies had shown that both the right odorant receptor protein and a shared, common partner protein called Orco must be present. The current team successfully engineered the genetic loss of Orco protein, which resulted in ants that could no longer perform some, if not all, pheromone-based social interactions.

Specifically, the altered young ants, unlike their nestmates without the changes, spent much of their time wandering out of the nest. They failed to interact with other members of the colony and were unable to forage and bring food back to the nest. Furthermore, mutant females no longer groomed males, a pre-mating behavior.

Harpegnathos worker ant tending to larva. Photo: Jürgen Liebig/ASU

Harpegnathos worker ant tending to larva. Photo: Jürgen Liebig/ASU

The current study is on the Indian jumping ant, Harpegnathos saltator, which is unlike in many ant species where only the queen can mate and pass on genes to the next generation. Any Harpegnathos female adult worker can be converted into a queen-like state in the absence of the queen or other queen-like workers.
This only works when the queen secretes a pheromone that suppresses the ability of workers to mate and lay eggs. If the queen is removed, the most aggressive female, after winning a series of antenna duels, transitions into a queen, and goes on to produce the progeny essential for colony survival.

The current study found that, without Orco, the females cannot process pheromones, which makes them much less likely to engage in dueling.

“This ant system allows dissecting the organization of a society in which social interactions of all individually marked colony members can be tracked easily,” Liebig added.

Another study relied on the fact that each cell (odorant receptor neuron) in the ant brain that can detect a given pheromone on the surface of the insect’s antennae shoots out extensions to a blob-like brain structure called a glomerulus. Information about that odor is processed there.

According to other studies, in insects such as mosquitoes, fruit flies and moths, the connections between odor receptors and glomeruli are “hard-wired,” i.e. their neural development do not rely on smells coming in and stimulating the odor receptor. But mammals appear to have odor receptor cells that home in and plug into the correct glomeruli based on the kind of odor receptors found on them. Clearly, actively smelling stuff encourages odor receptors to wire themselves to the right brain area in mice (and humans); in contrast the wiring is genetically preordained in flies, say the study authors.

The new research suggests that Harpegnathos ants, like mice and men, may also have evolved to have flexible nerve connections forming from receptor to glomerulus on the basis of activity. This means depending on the range of smells they experience, they can expand their repertoire of olfactory receptors for detecting pheromones. This flexibility is required for communication based on the pheromone sensitivity and resultant activity of their olfactory neurons, say the authors.

The research found that losing the crucial Orco gene left female ants, on average, with just 62 of the 275 glomeruli they would normally develop to process pheromone sensing.

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Here is some background on ant social life (from vanderbilt.edu)

Based on material from Arizona State University